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Neuroethology, its roots and future

Article  in  Journal of Comparative Physiology A · November 1999

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J Comp Physiol A (1999) 185: 389±392
REVIEW
H.-J. P¯uÈger á R. Menzel
Neuroethology, its roots and future
Accepted: 17 June 1999
Abstract Scholars in a particular scienti®c ®eld should
be familiar with its historical roots. Such knowledge will
put their own research into a historical perspective, and,
in addition, will allow them to assess current strengths
and weaknesses in their particular area of research. To
keep an exciting ®eld like neuroethology alive and close
to fast moving scienti®c frontiers, it is necessary to
constantly adapt and broaden its approaches to newly
emerging ideas from other ®elds, and to quickly incor-
porate new methodologies. The following article tries to
expose some of the roots of neuroethology, and, in ad-
dition, will present some evidence as to why the authors
think this ®eld needs a broader de®nition than that
formulated in the past. Doing so after the 5th Interna-
tional Congress of Neuroethology in San Diego in Au-
gust 1998 seems to the authors the most appropriate
time.
Introduction
The word neuroethology itself is a merger between
ethology, according to Konrad Lorenz (1981) ``the
comparative study of behavior which applies to the be-
havior of animals and humans'', and neurophysiology
(or neurobiology, to use a di€erent de®nition), ``the
study of the function of the nervous system''. Therefore,
in its simplest de®nition neuroethology is the study of
the neural mechanisms underlying behavior. Thus, it
was only when general knowledge of the morphology
and function of the nervous systems in humans and
animals became available and was accumulated in the
19th century by pioneers such as Ramon y Cajal,
H.-J. P¯uÈger (&) á R. Menzel
Freie UniversitaÈt Berlin, Fachbereich Biologie, Chemie,
Pharmazie, Institut fuÈr Biologie, Neurobiologie,
KoÈnigin-Luise-Str. 28/30, D-14195 Berlin, Germany
Ó Springer-Verlag 1999
Johannes MuÈller, and Emil du Bois-Reymond, that the
foundations were laid for linking behavior with events in
the nervous system.
Historical roots of behavioral biology
The ®eld of ethology was established by pioneers such as
Oskar Heinroth, Konrad Lorenz, Niko Tinbergen and
Karl von Frisch. Behavior was described and analyzed
by careful observation of animals in their natural habitat
or natural-like habitat in captivity. A major diculty in
any behavioral study, the high inter-individual vari-
ability of behavioral expressions, was reduced by fo-
cusing on particular forms of behavior and on the
selection of animal species. Rhythmic motor behaviors
(walking, ¯ying, swimming) and communicative behav-
iors (particularly in the context of courtship) were pre-
dominantly studied (see also Camhi 1984; Hoyle 1984;
Burrows 1996). These behaviors are to a great extent
inherited, and thus vary less between individuals. They
are released or controlled by rather ®xed stimuli and are
displayed by the animals rather stereotypically. Birds
and insects were the animals of choice by many
ethologists. Erich von Holst (1969, 1970) pioneered be-
havioral physiology (Verhaltensphysiologie) by focusing
on the elements of rhythmic behavior and examining the
function of the nervous system by localizing and ana-
lyzing the mechanisms of release and expression of these
elementary forms of behavior.
Ethologists developed the concepts of ``®xed action
patterns'' and ``sign stimuli'', a connection between
stimulus and response which could also be applied for
rather complex stimuli and elaborate behavioral pat-
terns. Both the strength and the weakness of classical
ethology is expressed in these concepts. On the one
hand, the focus on inherited behavior provided re-
searchers with valuable and reproducible data sets, but
on the other hand, guided them away from the other
major source of information underlying behavior ± in-
dividual learning. This aspect of behavioral biology was
390
studied intensively by the American school of experi-
mental psychology (behaviorism) (Skinner 1938; Hull
1943) and from a di€erent vantage point by the Russian
scientist Ivan Pavlov (1927). Behaviorism and Pavlov's
re¯exology dealt di€erently with behavior variability,
namely by bringing the animal to the laboratory,
reducing the complex environment to a small number of
external variables, and focusing on simple behavioral
patterns which are easily learned by the animal under
constrained conditions. Behaviorism has been extremely
valuable to behavioral biology by setting standards and
procedures for experimentation with animals. The ex-
perimental paradigms developed belong to the core of
modern behavioral biology, but neuroscience in general
and neuroethology in particular have gained little on the
conceptual level from behaviorism. This is because the
nervous system was conceptually eliminated by behav-
iorists on two grounds: (1) little can be said about the
nervous system when only input-output relationships are
studied, and (2) the output is thought to be fully con-
trolled by the input with the nervous system considered
to be a mere computational machine working according
to rules de®ned by the input. The concepts of ethology
were di€erent in this respect. The intrinsic productivity
of the nervous system was a basic notion; evidence was
established for spontaneous and input-independent ac-
tivity (``creativity'') of the nervous system. The depen-
dence of behavioral expressions on the internal status of
the animal (including the nervous system) was consid-
ered to be a major component in the expression of be-
havior and its variability. Thus, ethology has been
conceptually closer to the roots of modern cognitive
neuroscience, but the school of behaviorism has never-
theless helped enormously to avoid simple anthropo-
morphism and to establish a tradition of critical
experimentation.
Where are the questions coming from?
A bat ¯ying in total darkness; a bee orienting its ¯ight
path according to the polarized light pattern of the blue
sky; a blue jay ®nding stored food items at hundreds of
places ± behavior of animals confronts us with endless
questions about how this is achieved, what the under-
lying neural mechanisms are, how it was developed in
the course of evolution, and how it suits the animal's
needs. Neuroethologists ®nd their questions outdoors
but have to bring them into the laboratory for analysis.
This is a quite complex process, often with limited suc-
cess. The major questions need to be reduced to smaller,
workable ones, and there is a danger that the overriding
question might be lost by the constraints posed by lim-
ited methods. Probing the brain for neural correlates of
behavior imposes enormous restrictions and eliminates a
large proportion of the quite exciting problems, and thus
may reduce the relevance of the ®nding to the original
question. Although great methodological advances have
been made over the last 20 years it is still nearly
impossible to record intracellularly from neurons in a
performing animal, and aiming for particular individual
neurons is still limited to small nervous systems or
chopped-o€ (sliced) portions of bigger ones. Multiple
recordings from single neurons are possible only in rare
cases in behaving animals (e.g., place cells in hippo-
campus), and optical recording from ensembles of neu-
rons, a necessity for understanding the spatial and
temporal organization of a large number of neurons
during perceptional and behavioral performances, is still
a goal to be reached. The techniques are still rather
dissatisfying, compared to the secrets we want to un-
ravel. However, acceleration in the development of new
methods and the improvement of existing ones is im-
pressive. Therefore, we should continue to defend our
stronghold and search for questions by careful obser-
vation of animals in the wild, despite the unavoidable
consequence that we have to make so many compro-
mises.
Comparative studies
Each species has neighbors on an evolutionary scale, and
they are potential sources of information when we want
to understand a neural mechanism and the design
principles of the underlying networks. The reason is that
modi®cations induced by adapting to a particular eco-
logical niche can indicate which structures and functions
are more closely related to the performance involved.
Comparative studies are a speci®c realm of biological
sciences. Their value for the research process is not al-
ways fully appreciated, because arguments based on
comparison are correlative in nature and do not provide
a direct insight. However, analysis of (closely) related
species will open our eyes to the multitude of relation-
ships between structure and function, and provide hints
about neural strategies. For example the study of brain
structures in song and non-song birds provides insight
into how the nervous system had to undergo morpho-
logical and physiological changes to achieve the new
task of controlling singing in birds.
In favorable cases evolution might have led to the
development of specialized or reduced systems which
may be more easily accessible using techniques at hand.
Imprinting, for example, could be considered as a special
form of learning or a special form of epigenesis, and
such a mixed system provides us with the opportunity to
study the relationship between genetically controlled
developmental processes and experience-dependent
modi®cations.
Phylogenetically less advanced nervous systems come
with a smaller number of neurons and often solve rather
similar problems as do those with a large number of
neurons. For some unknown reason, such small nervous
systems often contain particularly large neurons which
can be individually identi®ed in favorable cases. Such a
situation is particularly appropriate for current electro-
physiological and anatomical techniques. Using such

systems, it has been possible to probe the rich capacity
of single, dedicated neurons. An additional advantage of
these systems is that they may produce, at least partially,
behavior under the restrained conditions in the labora-
tory and unravel the complex functions of individual
neurons.
The true ethologist may be taken aback when even
movements of internal organs such as intestines, hearts
or ventilatory muscles are subsumed under behavior
(Selverston and Moulins 1987; Harris-Warrick et al.
1992), but the fact is that without such studies, in¯uen-
tial and useful concepts such as those of the identi®ed
neuron and the central pattern generator could not have
been formulated.
The identi®ed neuron concept still proves useful for
circuit analysis, in which individual neurons are identi-
®ed as components of neural circuits by (1) their struc-
ture, (2) their physiological response, and (3) often by
their immunoreactivity (see Burrows 1996). Some par-
ticularly conspicuous neurons, better known as giant
neurons, could be identi®ed as command neurons whose
activity is necessary and sucient to trigger the initial
fast parts of, for example, the escape behaviors of
cray®sh, earthworms or squids (Edwards et al. 1999).
Studies on individual neurons have proven that for a
functional analysis it is necessary to know the identity of
a particular neuron not only with respect to its structure
or position in a neuronal circuit but also with respect to
its involvement with ion channels or intracellular sig-
naling pathways (see also Baro et al. 1997). This is a
completely new area which has not yet been fully inte-
grated into neuroethology.
However, the notion that single large neurons im-
plement rather stereotyped and fast functions of the
nervous system re¯ects only one aspect. Single, dedi-
cated large neurons can also represent a complex func-
tion (e.g., the rewarding components in appetitive
learning; Hammer 1993) and can be highly adaptive.
But neurons do not work in isolation, and function-
ally ¯exible ensembles of neurons are most likely the
building blocks of the nervous system (see below).
Learning and memory
Experience-dependent modi®cation of behavior has not
been at the center of ethology, and behaviorism has not
provided any concepts about the neural implementation
of learning and memory (see above). It is thus not sur-
prising that memory research routes derive from a dif-
ferent line of historical development in neuroscience. A
major question in neurology during the last century was
that of localization of function. Franz Josef Gall divided
the human cortex into 27 faculties, each residing in
di€erent parts of the cortex (phrenology). Although this
attempt was not backed up by experimental results or
objective observations, it initiated the search for mech-
anistic relationships between cognitive capacities and
brain structures. This view was substantiated by Brocca
391
and Wernecke who discovered areas in the temporal
lobe of the human brain essential for speech production
and recognition. Memory is a cognitive faculty, and the
question of where it resides in the brain was an impor-
tant one for neurologists who were exposed to severe
form of memory deterioration (e.g., Alzheimer,
Korsakov syndrome). From 1920 to 1950 Karl Lashley
(1942) dominated the scene. His failure to identify par-
ticular brain regions that were speci®c to, or necessary
for, memory storage called for alternative approaches in
memory research, and these were initiated by the psy-
chologist Donald Hebb (1949) and the neurologists
Brenda Milner and Wilder Pen®eld. Hebb postulated
that cognitive functions can indeed be distributed, be-
cause dynamic assemblies of neurons work together to
represent and store information, rather than a ®xed ar-
chitecture of nerve nets. Milner and Pen®eld discovered
the contribution of the hippocampal complex to recent
memory and the establishment of stable knowledge
about facts, faces and spatial layout, although old
memories were intact in patients who had their hippo-
campi dissected (Milner et al. 1998).
The notion that memory is not an integrated faculty
but is divided up both into temporal phases and with
respect to its contents, facilitated the identi®cation of
brain structures as substrates of these capacities. It was
only after these discoveries on patients that animal
studies again became important in memory research.
Meanwhile, we know that di€erent memory phases are a
property of nervous systems in general and somehow
re¯ect the self-organizing dynamics of the brain (Squire
1987). However, we barely understand why such dy-
namics evolved, and which ecological and behavioral
conditions can be better coped with when ®nal memory
formation is postponed. A typical domain of neuro-
ethological research, the comparative approach, will
provide us with clues to these puzzles, and observations
of animal performances under natural conditions will
ultimately help us to ask the right questions. Memory
contents determine the location of the memory trace not
only with respect to the sensory and motor channels
involved but also with respect to multimodal and cog-
nitive integration levels. For example, the hippocampus
or/and its phylogenetically related structures serve as an
integration and storage site for spatial orientation in
®sh, birds and mammals. Does this mean that neural
mechanisms underlying spatial representation and stor-
age in vertebrate brain are homologue faculties, which
are elaborated when behavioral demands are greater,
and reduced if less demanding behavioral strategies are
applied? Support for this notion comes from compara-
tive studies in food-storing and non-storing-birds
(Clayton and Krebs 1994). These studies are an excellent
case for the strength of neuroethological research. Not
only do we learn more about structure-function rela-
tionships, but we also gain insights into the evolutionary
process leading to higher brain performances.
Following this research strategy we might in the fu-
ture even understand why and how declarative forms of
392
memory in humans (those memories which we con-
sciously recollect) are related to the same brain struc-
ture, the hippocampus.
Single neuron versus ensembles of neurons
The concept of the single neuron being the substrate of
complex integration and decision making in the brain
reminds us of the ethological notion of sign stimuli and
innate release mechanisms. Would it not be wonderful if
nervous systems had the sign stimuli/release mechanisms
implemented in superneurons residing with a network of
handshaking cells in a hierarchically organized nervous
system? Indeed, there are neurons which cause the ani-
mal to perform a fully integrated piece of behavior (e.g.,
tail¯ip in decapods; Edwards et al. 1999) when one of
them produces one spike. There are also neurons which
respond rather selectively to particular combinations of
inputs (e.g., face neurons), and ± as mentioned above ±
there is a neuron that serves the reward function in ap-
petitive learning (the VUMmx1 in honeybees). Are these
dedicated neurons exclusive models of brain functions?
Certainly not, since overwhelming evidence indicates
that many neurons have to co-operate in the extraction
and coding of sensory features and the control of motor
patterns. The response pro®le of each of these neurons is
determined by many other neurons, and this interactive
process can be highly dynamic. But neural processing is
likely to be even more dynamic, leaving each single
neuron only the capacity of being a member in an as-
sembly, from which transiently interacting groups of
neurons are selected. Group selection on the basis of
variability at the level of single neurons resembles in-
teresting formal features of evolutionary processing
(neural Darwinism; Edelman 1993), and has been pro-
posed to explain the fact that interactive nets of many
rather similar, non-dedicated neurons appear to be re-
sponsible for feature extracting and coding.
Again, the comparative attitude in neuroethology
and the fascination of researchers by the multitude of
nervous systems as they appear at all phylogenetic levels
will provide us with most encouraging perspectives. Is
the proportion of non-dedicated neurons assembling in
¯exible groups related to the complexity of neural per-
formance, and does it depend on the phylogenetic level?
Do di€erent organizational principles of nervous sys-
tems (e.g., in invertebrates versus vertebrates; in di€er-
ent groups of vertebrates) lead to di€erent proportions
along the scale from dedicated to non-dedicated neu-
rons, from morphologically composed circuits to ¯exible
and multifunctional aggregates, and from specialized
solutions to productive compositions with emerging
properties? It is obvious that theories of brain functions
capture only small parts of these overwhelming prob-
View publication stats
lems (Singer and Gray 1995). The analogy with a com-
puter has been creative and stimulating, but it also limits
the view to pre-designed, restricted circuits. The call for
more general theories of nervous functions is certainly
one of the most pressing ones, and again the compara-
tive attitude of neuroethologists with their conceptual
foundations in evolutionary theory may be a creative
driving force behind the pursuit of such a theory.
Acknowledgements The authors would like to express their grati-
tude to Mary Wurm for helping with the English manuscript, and
Sabine Funke for expert secretarial work.
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